Hydrogen sulfide: a versatile regulator of environmental stress in plants

Acta Physiologiae Plantarum

Volumn 38, Issue 1, 2016, Pages 1-13

  Guo, Hongming ^a   Xiao, Tianyu ^a   Zhou, Heng ^a   Xie, Yanjie ^a   Shen, Wenbiao ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Cys desulfhydrases mechanism; Hydrogen sulfide signal molecule

Indexed keywords

EID: 84951268333     PISSN: 01375881     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11738-015-2038-x     Document Type: Review

References (109)

1. Aida K, Tokuyama T, Uemura T (1969) The role of cysteine desulphhydrase and cysteine synthase in the evolution of hydrogen sulphide in pantothenic acid deficient yeast. Antonie Van Leeuwenhoek 35(Suppl 1):15–16
2. Álvarez C, Bermúdez MÁ, Romero LC, Gotor C, García I (2012a) Cysteine homeostasis plays an essential role in plant immunity. New Phytol 193:165–177
3. Álvarez C, Calo L, Romero LC, García I, Gotor C (2010) An O-acetylserine(thiol)lyase homolog with l-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152:656–669
4. Álvarez C, García I, Moreno I, Pérez-Pérez ME, Crespo JL, Romero LC, Gotor C (2012b) Cysteine-generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis. Plant Cell 24:4621–4634
5. Aroca A, Serna A, Gotor C, Romero LC (2015) S-Sulfhydration: a cystein posttranslational modification in plant systems. Plant Physiol 168:334–342
6. Astier J, Rasul S, Koen E, Manzoor H, Besson-Bard A, Lamotte O, Jeandroz S, Durner J, Lindermayr C, Wendehenne D (2011) S-Nitrosylation: an emerging post-translational protein modification in plants. Plant Sci 181:527–533
7. Barroso C, Vega JM, Gotor C (1995) A new member of the cytosolic O-acetylserine(thiol)lyase gene family in Arabidopsis thaliana. FEBS Lett 365:1–5
8. Baskar R, Bian J (2011) Hydrogen sulfide gas has cell growth regulatory role. Eur J Pharmacol 656:5–9
9. Beja-Tal S, Borochov A (1994) Age-related changes in biochemical and physical properties of carnation petal plasma membranes. J Plant Physiol 143:195–199
10. Bonner ER, Cahoon RE, Knapke SM, Jez JM (2005) Molecular basis of cysteine biosynthesis in plants: structural and functional analysis of O-acetylserine sulfhydrylase from Arabidopsis thaliana. J Biol Chem 280:38803–38813
11. Borochov A, Cho MH, Boss WF (1994) Plasma membrane lipid metabolism of petunia petals during senescence. Physiol Plant 90:279–284
12. Borochov A, Woodson WR (1989) Physiology and biochemistry of flower petal senescence. Hortic Rev 11:15–43
13. Boyer JS (1982) Plant productivity and environment. Science 218:443–448
14. 2 synthesis. Plant J 45:113–122
15. Burandt P, Schmidt A, Papenbrock J (2002) Three O-acetyl-l-serine(thiol)lyase isoenzymes from Arabidopsis catalyse cysteine synthesis and cysteine desulfuration at different pH values. J Plant Physiol 159:111–119
16. Calderwood A, Kopriva S (2014) Hydrogen sulfide in plants: from dissipation of excess sulfur to signaling molecule. Nitric Oxide 41:72–78
17. Chaerle L, Saibo N, Van Der Straeten D (2005) Tuning the pores: towards engineering plants for improved water use efficiency. Trends Biotechnol 23:308–315
18. Chen J, Wang WH, Wu FH, You CY, Liu TW, Dong XJ, He JX, Zheng HL (2013) Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant Soil 362:301–318
19. Cooper CE, Brown GC (2008) The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance. J Bioenerg Biomembr 40:533–539
20. Dawood M, Cao F, Jiahanqir MM, Zhang G, Wu F (2012) Alleviation of aluminum toxicity by hydrogen sulfide is related to elevated ATPase, and suppressed aluminum uptake and oxidative stress in barley. J Hazard Mater 209–210:121–128
21. Dorman DC, Moulin FJ-M, McManus BE, Mahle KC, Jmmes RA, Struve MF (2001) Cytochrome oxidase inhibition induced by acute hydrogen sulfide inhalation: correlation with tissue sulfide concentrations in the rat brain, liver, lung, and nasal epithelium. Toxicol Sci 65:18–25
22. 6+ tolerance in Setaria italica. Chin J Cell Biol 36:758–765
23. Ferreira-Silva SL, Voigt EL, Silva EN, Maia JM, Aragão TC, Silveira JAG (2012) Partial oxidative protection by enzymatic and non-enzymatic components in cashew leaves under high salinity. Biol Plant 56:172–176
24. García-Mata C, Lamattina L (2010) Hydrogen sulfide, a novel gasotransmitter involved in guard cell signaling. New Phytol 188:977–984
25. García-Mata C, Lamattina L (2013) Gssotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci 201(202):66–73
26. Gupta KJ (2011) Protein S-nitrosylation in plants: photorespiratory metabolism and NO signaling. Sci Signal 4(154):jc1. doi:10.1126/scisignal.2001404
27. Hancock JT, Whiteman M (2014) Hydrogen sulfide and cell signaling: team player or referee? Plant Physiol Biochem 78:37–42
28. Hanumappa M, Nguyen HT (2010) Genetic approaches toward improving heat tolerance in plants. In: Jenks MA, Wood AJ (eds) Genes for plant abiotic stress. Blackwell Publishing, Oxford, UK, pp 221–260
29. Harrington HM, Smith IK (1980) Cysteine metabolism in cultured tobacco cells. Plant Physiol 65:151–155
30. Hell R, Bork C, Bogdanova N, Frolov I, Hauschild R (1994) Isolation and characterization of two cDNAs encoding for compartment specific isoforms of O-acetylserine (thiol) lyase from Arabidopsis thaliana. FEBS Lett 351:257–262
31. Helmy N, Prip-Buus C, Vons C, Lenoir V, Abou-Hamdan A, Guedouari-Bounihi H, Lombès A, Bouillaud F (2014) Oxidation of hydrogen sulfide by human liver mitochondria. Nitric Oxide 41:105–112
32. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6:150–166
33. Hess DT, Stamler JS (2012) Regulation by S-nitrosylation of protein posttranslational modification. J Biol Chem 287:4411–4418
34. Hesse H, Lipke J, Altmann T, Höfgen R (1999) Molecular cloning and expression analyses of mitochondrial and plastidic isoforms of cysteine synthase (O-acetylserine(thiol)lyase) from Arabidopsis thaliana. Amino Acids 16:113–131
35. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908
36. 2 in jasmonic acid-induced stomatal closure in Vicia faba. Chin Bull Bot 46:396–406
37. Hu JL, Huang XH, Chen LC, Sun XW, Lu CM, Zhang LX, Wang YC, Zuo JR (2015) Site-specific nitrosoproteomic identification of endogenously S-nitrosylated proteins in Arabidopsis. Plant Physiol 167:1734–1746
38. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH (2001) Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 3:193–197
39. Jin ZP, Shen JJ, Qiao ZJ, Yang GD, Wang R, Pei YX (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 414:481–486
40. Jin ZP, Xue SW, Luo YN, Tian BH, Fang HH, Li H, Pei YX (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem 62:41–46
41. Jost R, Berkowitz O, Wirtz M, Hopkins L, Hawkesford MJ, Hell R (2000) Genomic and functional characterization of the oas gene family encoding O-acetylserine (thiol) lyases, enzymes catalyzing the final step in cysteine biosynthesis in Arabidopsis thaliana. Gene 253:237–247
42. 2S and its role in redox signaling. Biochim Biophys Acta 1844:1355–1366
43. Kida K, Yamada M, Tokuda K, Marutani E, Kakinohana M, Kaneki M, Ichinose F (2011) Inhaled hydrogen sulfide prevents neurodegeneration and movement disorder in a mouse model of Parkinson’s disease. Antioxid Redox Signal 15:343–352
44. Kimura H (2000) Hydrogen sulfide induces cyclic AMP and modulates the NMDA recrptor. Biochem Biophys Res Commun 267:129–133
45. Kimura H (2014) The physiological role of hydrogen sulfide and beyond. Nitric Oxide 41:4–10
46. Kimura Y, Kimura H (2004) Hydrogen sulfide protects neurons from oxidative stress. FASEB J 18:1165–1167
47. Knight H (2000) Calcium signaling during abiotic stress in plants. Int Rev Cytol 195:269–324
48. Kolluru GK, Shen X, Bir SC, Kevil CG (2013) Hydrogen sulfide chemical biology: pathophysiological roles and detection. Nitric Oxide 35:5–20
49. Kubo S, Kurokawa Y, Doe I, Masuko T, Sekiguchi F, Kawabata A (2007) Hydrogen sulfide inhibits activity of three isoforms of recombinant nitric oxide synthase. Toxicology 241:92–97
50. Kushnir S, Babiychuk E, Storozhenko S, Davey MW, Papenbrock J, De Rycke R, Engler G, Stephan UW, Lange H, Kispal G, Lill R, Van Montagu M (2001) A Mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13:89–100
51. + loss in seedlings of Medicago sativa. Plant Sci 225:117–129
52. Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:628–695
53. Leon S, Tournaine B, Briat JF, Lobreaux S (2002) The AtNFS2 gene from Arabidopsis thaliana encodes a NifS-like plastidial cysteine desulphurase. Biochem J 366:557–564
54. Li ZG, Ding XJ, Du PF (2013a) Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. J Plant Physiol 170:741–747
55. 2+ and calmodulin. Plant Sci 185–186:185–189
56. + antiporter system in the hydrogen peroxide-dependent manner in salt-stress Arabidopsis thaliana root. Protoplasma 251:899–912
57. Li L, Wang YQ, Shen WB (2012) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25:617–631
58. Li L, Whiteman M, Guan YY, Neo KL, Cheng Y, Lee SW, Zhao Y, Baskar R, Tan CH, Moore PK (2008) Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): new insights into the biology of hydrogen sulfide. Circulation 117:2351–2360
59. Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013b) Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36:1564–1572
60. Lin YT, Li MY, Cui WT, Lu W, Shen WB (2012) Haem oxygenase-1 is involved in hydrogen sulfide-induced cucumber adventitious root formation. J Plant Growth Regul 31:519–528
61. Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930
62. Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, Wood ME, Whiteman M, Hancock JT (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 48:931–935
63. Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulphide: environmental factor or signaling molecule? Plant Cell Environ 36:1607–1616
64. Lisjak M, Teklic T, Wilson ID, Wood ME, Whiteman M, Hancock JT (2011) Hydrogen sulfide effects on stomatal apertures. Plant Signal Behav 6:1444–1446
65. Mancardi D, Penna C, Merlino A, Del Soldato P, Wink DA, Pagliaro P (2009) Physiological and pharmacological features of the novel gasotransmitter: hydrogen sulfide. Biochim Biophys Acta 1787:864–872
66. 2S Signals through protein S-sulfhydration. Sci Signal 2:72
67. Nagasawa T, Ishii T, Kumagai H, Yamada H (1985) d-Cysteine desulfhydrase of Escherichia coli. Purification and characterization. Eur J Biochem 153:541–551
68. Nagasawa T, Ishii T, Yamada H (1988) Physiological comparison of d-cysteine desulfhydrase of Escherichia coli with 3-chloro-d-alanine dehydrochlorinase of Pseudomonas putida CR 1–1. Arch Microbiol 149:413–416
69. Olas B (2015) Hydrogen sulfide in signaling pathways. Clin Chim Acta 439:212–218
70. Paliyath G, Droillard MJ (1992) The mechanisms of membrane deterioration and disassembly during senescence. Plant Physiol Biochem 30:789–812
71. 2S-releasing enzymes of higher plants: from the field to the test tube and back. Plant Biol 9:582–588
72. Pilon-Smits EA, Garifullina GF, Abdel-Ghany S, Kato S, Mihara H, Hale KL, Burkhead JL, Esaki N, Kurihara T, Pilon M (2002) Characterization of a NifS-like chloroplast protein from Arabidopsis. Implications for its role in sulfur and selenium metabolism. Plant Physiol 130:1309–1318
73. Polhemus DJ, Lefer DJ (2014) Emergence of hydrogen sulfide as an endogenous gaseous signaling molecule in cardiovascular disease. Circ Res 114:730–737
74. Rennenberg H (1983) Cysteine desulfhydrase activity in cucurbit plants: simulation by preincubation with l- and d-cysteine. Phytochemistry 22:1557–1560
75. Rennenberg H, Arabatzis N, Grundel I (1987) Cysteine desulphydrase activity in higher plants: evidence for the action of l- and d-cysteine specific enzymes. Phytochemistry 26:1583–1589
76. 2S emission in cucurbit plants. Plant Physiol 71:269–275
77. Riemenschneider A, Weqele R, Schmidt A, Papenbrock J (2005) Isolation and characterization of a d-cysteine desulfhydrase protein from Arabidopsis thaliana. FEBS J 272:1291–1304
78. Romero LC, Aroca MA, Serna A, Gotor C (2013a) Proteomic analysis of endogenous S-sulfhydration in Arabidopsis thaliana. Nitric Oxide 31:S23
79. Romero LC, Garcia I, Gotor C (2013b) l-Cysteine desulfhydrase1 modulates the generation of the signaling molecule sulfide in plant cytosol. Plant Signal Behav 8:e24007
80. Rubinstein B (2000) Regulation of cell death in flower petals. Plant Mol Biol 44:303–318
81. Schmidt A (1982) A cysteine desulfhydrase from spinach leaves specific for d-cysteine. Zeitschrift fr Pflanzenphysiologie 107:301–312
82. Schmidt A, Erdle I (1983) A cysteine desulfhydrase specific for d-cysteine from the green alga Chlorella fusca. Zeitschrift für Naturforschung C 38:428–435
83. Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365
84. Scuffi D, Núñez A, Laspina N, Gotor C, Lamattina L, Garcia-Mata C (2014) Hydrogen sulfide generated by l-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiol 166:2065–2076
85. Sen N, Paul BD, Gadalla MM, Mustafa AK, Sen T, Xu R, Kin S, Snyder SH (2012) Hydrogen sulfide-linked Sulfhydration of NF-κB mediates its antiapoptotic actions. Mol Cell 45(1):13–24
86. Shan C, Liu H, Zhao L, Wang X (2014) Effects of exogenous hydrogen sulfide on the redox states of ascorbate and glutathione in maize leaves under salt stress. Biol Plant 58:169–173
87. Shi Q, Ding F, Wang X, Wei M (2007) Exogenous nitric oxide protects cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem 45:542–550
88. Shi HT, Ye TT, Chan ZL (2014) Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 74:99–107
89. Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, Ishii K (2009) 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal 11:703–714
90. Singh VP, Singh S, Kumar J, Prasad SM (2015) Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate–glutathione cycle: possible involvement of nitric oxide. J Plant Physiol 181:20–29
91. Stamler JS, Lamas S, Fang FC (2001) Nitrosylation, the prototypic redox-based signaling mechanism. Cell 106:675–683
92. Sun J, Wang R, Zhang X, Yu Y, Zhao R, Li Z, Chen S (2013) Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiol Biochem 65:67–74
93. Wahid A, Gelani S, Ashrf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223
94. 2S be the third endogenous gaseous transmitter? FASEB J 16:1792–1798
95. Wang Y, Li L, Cui W, Xu S, Shen W, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351:107–119
96. Wang BL, Shi L, Li YX, Zhang WH (2010) Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings. Planta 231:1301–1309
97. Wang Y, Yun BW, Kwon E, Hong JK, Yoon J, Loake GJ (2006) S-Nitrosylation: an emerging redox-based post-translational modification in plants. J Exp Bot 57:1777–1784
98. Wirtz M, Droux M, Hell R (2004) O-Acetylserine(thiol)lyase: an enigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana. J Exp Bot 55:1785–1798
99. Xie YJ, Lai DW, Mao Y, Zhang W, Shen WB, Guan RZ (2013a) Molecular cloning, characterization, and expression analysis of a novel gene encoding l-cysteine desulfhydrase from Brassica napus. Mol Biotechnol 54:737–746
100. Xie YJ, Zhang C, Lai DW, Sun Y, Samma MK, Zhang J, Shen WB (2013b) Hydrogen sulfide delays GA-triggered programmed cell death in wheat aleurone layers by the modulation of glutathione homeostasis and heme oxygenase-1 expression. J Plant Physiol 171:53–62
101. Xu S, Liu Z, Liu P (2014) Targeting hydrogen sulfide as a promising therapeutic strategy for atherosclerosis. Int J Cardiol 172:313–317
102. Yang G, Zhao K, Ju Y, Mani S, Cao Q, Puukila S, Khaper N, Wu L, Wang R (2013) Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2. Antioxid Redox Signal 18:1906–1919
103. Yoo KS, Ok SH, Jeong BC, Jung KW, Cui MH, Hyoung S, Lee MR, Song HK, Shin JS (2011) Single cystathionine β-synthase domain-containing proteins modulate development by regulating the thioredoxin system in Arabidopsis. Plant Cell 23:3577–3594
104. Yruela I (2005) Copper in plants. Braz J Plant Physiol 17:145–156
105. Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol 50:1518–1529
106. Zhang H, Hu SL, Zhang ZJ, Hu LY, Jiang CX, Wei ZJ, Liu J, Wang HL, Jiang ST (2011) Hydrogen sulfide acts as a regulator of flower senescence in plants. Postharvest Biol Technol 60:251–257
107. Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094
108. Zhang H, Wang MJ, Hu LY, Wang SH, Hu KD, Bao LJ, Luo JP (2010) Hydrogen sulfide promotes wheat seed germination under osmotic stress. Russ J Plant Physiol 57:532–539
109. 2S as a novel endogenous gaseous KATP channel opener. EMBO J 20:6008–6016